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Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells

Physiological and pathological morphogenetic events involve a wide array of collective movements, suggesting that multicellular arrangements confer biochemical and biomechanical properties contributing to tissue-scale organization. The Ciona cardiopharyngeal progenitors provide the simplest model of...

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Autores principales: Bernadskaya, Yelena Y, Yue, Haicen, Copos, Calina, Christiaen, Lionel, Mogilner, Alex
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8700272/
https://www.ncbi.nlm.nih.gov/pubmed/34842140
http://dx.doi.org/10.7554/eLife.70977
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author Bernadskaya, Yelena Y
Yue, Haicen
Copos, Calina
Christiaen, Lionel
Mogilner, Alex
author_facet Bernadskaya, Yelena Y
Yue, Haicen
Copos, Calina
Christiaen, Lionel
Mogilner, Alex
author_sort Bernadskaya, Yelena Y
collection PubMed
description Physiological and pathological morphogenetic events involve a wide array of collective movements, suggesting that multicellular arrangements confer biochemical and biomechanical properties contributing to tissue-scale organization. The Ciona cardiopharyngeal progenitors provide the simplest model of collective cell migration, with cohesive bilateral cell pairs polarized along the leader-trailer migration path while moving between the ventral epidermis and trunk endoderm. We use the Cellular Potts Model to computationally probe the distributions of forces consistent with shapes and collective polarity of migrating cell pairs. Combining computational modeling, confocal microscopy, and molecular perturbations, we identify cardiopharyngeal progenitors as the simplest cell collective maintaining supracellular polarity with differential distributions of protrusive forces, cell-matrix adhesion, and myosin-based retraction forces along the leader-trailer axis. 4D simulations and experimental observations suggest that cell-cell communication helps establish a hierarchy to align collective polarity with the direction of migration, as observed with three or more cells in silico and in vivo. Our approach reveals emerging properties of the migrating collective: cell pairs are more persistent, migrating longer distances, and presumably with higher accuracy. Simulations suggest that cell pairs can overcome mechanical resistance of the trunk endoderm more effectively when they are polarized collectively. We propose that polarized supracellular organization of cardiopharyngeal progenitors confers emergent physical properties that determine mechanical interactions with their environment during morphogenesis.
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spelling pubmed-87002722022-01-04 Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells Bernadskaya, Yelena Y Yue, Haicen Copos, Calina Christiaen, Lionel Mogilner, Alex eLife Computational and Systems Biology Physiological and pathological morphogenetic events involve a wide array of collective movements, suggesting that multicellular arrangements confer biochemical and biomechanical properties contributing to tissue-scale organization. The Ciona cardiopharyngeal progenitors provide the simplest model of collective cell migration, with cohesive bilateral cell pairs polarized along the leader-trailer migration path while moving between the ventral epidermis and trunk endoderm. We use the Cellular Potts Model to computationally probe the distributions of forces consistent with shapes and collective polarity of migrating cell pairs. Combining computational modeling, confocal microscopy, and molecular perturbations, we identify cardiopharyngeal progenitors as the simplest cell collective maintaining supracellular polarity with differential distributions of protrusive forces, cell-matrix adhesion, and myosin-based retraction forces along the leader-trailer axis. 4D simulations and experimental observations suggest that cell-cell communication helps establish a hierarchy to align collective polarity with the direction of migration, as observed with three or more cells in silico and in vivo. Our approach reveals emerging properties of the migrating collective: cell pairs are more persistent, migrating longer distances, and presumably with higher accuracy. Simulations suggest that cell pairs can overcome mechanical resistance of the trunk endoderm more effectively when they are polarized collectively. We propose that polarized supracellular organization of cardiopharyngeal progenitors confers emergent physical properties that determine mechanical interactions with their environment during morphogenesis. eLife Sciences Publications, Ltd 2021-11-29 /pmc/articles/PMC8700272/ /pubmed/34842140 http://dx.doi.org/10.7554/eLife.70977 Text en © 2021, Bernadskaya et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Computational and Systems Biology
Bernadskaya, Yelena Y
Yue, Haicen
Copos, Calina
Christiaen, Lionel
Mogilner, Alex
Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
title Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
title_full Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
title_fullStr Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
title_full_unstemmed Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
title_short Supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
title_sort supracellular organization confers directionality and mechanical potency to migrating pairs of cardiopharyngeal progenitor cells
topic Computational and Systems Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8700272/
https://www.ncbi.nlm.nih.gov/pubmed/34842140
http://dx.doi.org/10.7554/eLife.70977
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